Arm autotomy and arm branching pattern as anti-predatory adaptations in stalked and stalkless crinoids

136

Over the last 15 years a striking pattern of diversification has been documented in the fossil record of benthic marine invertebrates. Higher taxa (orders) tend to originate onshore, diversify offshore, and retreat into deepwater environments. Previous studies attribute this macroevolutionary pattern to a variety of causes, foremost among them the role of nearshore disturbance in providing opportunities for the evolution of novel forms accorded ordinal rank. Our analysis of the post-Paleozoic record of ordinal first appearances indicates that the onshore preference of ordinal origination occurred only in the Mesozoic prior to the Turonian stage of the Cretaceous, a period characterized by relatively frequent anoxic͞dysoxic bottom conditions in deeper marine environments. Later, in the Cretaceous and Cenozoic, ordinal origination of benthic organisms did not occur exclusively, or even preferentially, in onshore environments. This change in environmental pattern of ordinal origination roughly correlates with Late Cretaceous: (i) decline in anoxia͞dysoxia in offshore benthic environments; (ii) extinction of faunas associated with dysoxic conditions; (iii) increase in bioturbation with the expansion of deep burrowing forms into offshore environments; and (iv) offshore expansion of bryozoan diversity. We also advance a separate argument that the Cenomanian͞Turonian and latest Paleocene global events eliminated much of the deep-water benthos. This requires a more recent origin of modern vent and deep-sea faunas, from shallower water refugia, than the Paleozoic or early Mesozoic origin of these faunas suggested by other workers.An onshore to offshore evolutionary pattern is evident in benthic marine invertebrate clades of the Paleozoic (1, 2) and post-Paleozoic (3-7) age. Ordinal rank taxa are observed to originate onshore, diversify offshore, and eventually relinquish nearshore habitat. This pattern has been attributed to a number of factors (5), the most clearly articulated of which invokes higher disturbance in shallow marine environments as a mechanism that eliminates niche incumbents, permitting the evolution of novel attributes subsequently recognized as new, ordinal rank, higher taxa (8). Expansion across the shelf to deeper offshore habitats then accompanies diversification of the clade (3-6). Explanations advanced for the subsequent offshore retreat of taxonomic groups include the evolution of new predators (9) and more effective competitors (10) in the nearshore environment. Thus, the nearshore is thought of as a source of evolutionary novelty resulting from disturbance, and subsidiary aspects of the pattern, such as offshore retreat, are thought of as responses to ecological interaction associated with the appearance of evolutionary novelty in the nearshore.In this paper we argue (i) that a component of the postPaleozoic onshore͞offshore evolutionary pattern (3-7) resulted from the preferential influence of anoxic͞dysoxic bottom conditions (a͞dbc) on offshore faunas; (ii) that a͞dbc were prevalent in...

Section: Anoxic Events and The Age Of The Modern Deep-sea Faunamentioning

confidence: 99%

Oxygen and evolutionary patterns in the sea: Onshore/offshore trends and recent recruitment of deep-sea faunas

Jacobs

Lindberg

1998

136

“…Although predation by fish on crinoids and its evolutionary consequences have received the most attention (21)(22)(23)(24)(25)(26)(27), sparse data indicated that crinoids may be the prey of benthic invertebrates (28), most notably sea urchins (17-19, 29, 30). Recently it has been shown that during the Triassic, the radiation of cidaroid sea urchins capable of handling the crinoid skeleton coincided with high frequency of bite marks on crinoids likely produced by the jaw apparatus of these sea urchins (18).…”

mentioning

confidence: 99%

“…The bite traces we report were culled from among other traces on the basis of their similarity to traces found on crinoid skeletal elements retrieved from the guts and feces of extant cidaroids (17,18). Furthermore, we collected data for stalk fragments only, as stalks are most likely to be bitten by benthic organisms, such as sea urchins, rather than fish, which have been shown to focus on crinoid arms and cups (21)(22)(23)(24)(25). The repeated co-occurrence of sea urchins at the localities from which crinoids with bite marks were recovered is also consistent with this interpretation.…”

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confidence: 99%

Predator-induced macroevolutionary trends in Mesozoic crinoids

Gorzelak

Salamon

Baumiller

2012

Sea urchins are a major component of recent marine communities where they exert a key role as grazers and benthic predators. However, their impact on past marine organisms, such as crinoids, is hard to infer in the fossil record. Analysis of bite mark frequencies on crinoid columnals and comprehensive genus-level diversity data provide unique insights into the importance of sea urchin predation through geologic time. These data show that over the Mesozoic, predation intensity on crinoids, as measured by bite mark frequencies on columnals, changed in step with diversity of sea urchins. Moreover, Mesozoic diversity changes in the predatory sea urchins show a positive correlation with diversity of motile crinoids and a negative correlation with diversity of sessile crinoids, consistent with a crinoid motility representing an effective escape strategy. We contend that the Mesozoic diversity history of crinoids likely represents a macroevolutionary response to changes in sea urchin predation pressure and that it may have set the stage for the recent pattern of crinoid diversity in which motile forms greatly predominate and sessile forms are restricted to deep-water refugia.echinoderms | escalation | macroecology I t has long been hypothesized that predator-prey interactions represent a significant driving force of evolutionary change in the history of life (1-4). However, not only is predation itself hard to detect in the fossil record, which makes it difficult to ascertain its intensity over geologic time, but macroevolutionary predictions of the hypothesis are far from simple (5-13). Recent sea urchins (Echinoidea), are known to play a key role in shallow sea ecosystems as grazers and benthic predators that can modify the distribution, abundance, and species composition of coral and algal reef communities (14-16); however, only few data have hinted at the importance of sea urchins to crinoids (17)(18)(19).Crinoids (Crinoidea), commonly known as sea lilies or feather stars, were one of the dominant components of many shallow-sea environments through much of geologic history and a key contributor to the sedimentary record (20). Although predation by fish on crinoids and its evolutionary consequences have received the most attention (21-27), sparse data indicated that crinoids may be the prey of benthic invertebrates (28), most notably sea urchins (17-19, 29, 30). Recently it has been shown that during the Triassic, the radiation of cidaroid sea urchins capable of handling the crinoid skeleton coincided with high frequency of bite marks on crinoids likely produced by the jaw apparatus of these sea urchins (18). Because it was also during the Triassic that various modes of active and passive motility appeared among crinoids, a group that throughout its rich pre-Triassic history was almost exclusively sessile, it was argued that crinoid motility, an effective escape strategy against benthic predation, was an evolutionary response to echinoid predation (18).The hypothesized evolutionary response of crinoids to benthic pr...

“…Data on fossil and extant crinoids, commonly known as sea lilies and feather stars (Echinodermata), indicate that they suffer from predation by fishes, and numerous evolutionary trends have been ascribed to such interactions (5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15). Among these are (i) crawling and swimming abilities in comatulids (6), (ii) choice of semicryptic habits and nocturnal-diurnal behavior among comatulids (6), (iii) increasing plate thickness and spinosity among Paleozoic crinoids (9), (iv) offshore displacement of late Mesozoic/Cenozoic stalked crinoids (11), and (v) origin of autotomy (shedding) planes in the stalk and arms (13). Some of these trends have served as examples of dramatic change in marine ecosystems, such as the Mesozoic marine revolution (MMR) (2,16) and the middle-Paleozoic marine revolution (9).…”

mentioning

confidence: 99%

Post-Paleozoic crinoid radiation in response to benthic predation preceded the Mesozoic marine revolution

Baumiller

Salamon

Gorzelak

et al. 2010

137

116

It has been argued that increases in predation over geological time should result in increases in defensive adaptations in prey taxa. Recent in situ and laboratory observations indicate that cidaroid sea urchins feed on live stalked crinoids, leaving distinct bite marks on their skeletal elements. Similar bite marks on fossil crinoids from Poland strongly suggest that these animals have been subject to echinoid predation since the Triassic. Following their near-demise during the end-Permian extinction, crinoids underwent a major evolutionary radiation during the Middle-Late Triassic that produced distinct morphological and behavioral novelties, particularly motile taxa that contrasted strongly with the predominantly sessile Paleozoic crinoid faunas. We suggest that the appearance and subsequent evolutionary success of motile crinoids were related to benthic predation by post-Paleozoic echinoids with their stronger and more active feeding apparatus and that, in the case of crinoids, the predation-driven Mesozoic marine revolution started earlier than in other groups, perhaps soon after the endPermian extinction.macroecology | macroevolution | predation | escalation | cidaroids P redator-prey interactions may represent a significant driving force of evolutionary change (1-4), but predation and its consequences are often difficult to assess in Recent communities and even more so in the fossil record. Data on fossil and extant crinoids, commonly known as sea lilies and feather stars (Echinodermata), indicate that they suffer from predation by fishes, and numerous evolutionary trends have been ascribed to such interactions (5-15). Among these are (i) crawling and swimming abilities in comatulids (6), (ii) choice of semicryptic habits and nocturnal-diurnal behavior among comatulids (6), (iii) increasing plate thickness and spinosity among Paleozoic crinoids (9), (iv) offshore displacement of late Mesozoic/Cenozoic stalked crinoids (11), and (v) origin of autotomy (shedding) planes in the stalk and arms (13). Some of these trends have served as examples of dramatic change in marine ecosystems, such as the Mesozoic marine revolution (MMR) (2, 16) and the middle-Paleozoic marine revolution (9).Although predation by fish has received the most attention, crinoids may be the prey of other organisms, most notably benthic invertebrates. Until recently, few data hinted at the importance of benthic predators to crinoids, including a swimming response in a comatulid when perturbed by the predatory sea star Pycnopodia helianthoides (17), the presence of crinoid pinnulars in the gut of the goniasterid Plinthaster dentatus (18), and a crinoid arm observed in the claw of the crab Oregonia gracilis (17). Recently, submersible studies of stalked crinoids belonging to the Isocrinidae have revealed that they are prey to cidaroids, or pencil urchins. Evidence for this interaction includes (i) in situ observations of cidaroids among large aggregations of motile isocrinid sea lilies (Neocrinus decorus and Endoxocrinus parrae), (ii) proximi...